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Microbiological Research 215 (2018) 76–88

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Microbiological Research
journal homepage: www.elsevier.com/locate/micres

Matricaria genus as a source of antimicrobial agents: From farm to pharmacy T


and food applications
Mehdi Sharifi-Rada, Jolanta Nazarukb, Letizia Politoc, Maria Flaviana Bezerra Morais-Bragad,
⁎⁎
Janaína Esmeraldo Rochad, Henrique Douglas Melo Coutinhod, Bahare Salehie,f, ,
Giulia Tabanellig, Chiara Montanarig, María del Mar Contrerash, Zubaida Yousafi,
⁎⁎⁎ ⁎
William N. Setzerj, Deepa R. Vermak, Miquel Martorelll, , Antoni Suredam, Javad Sharifi-Radn,o,
a
Department of Medical Parasitology, Zabol University of Medical Sciences, Zabol, 61663-335, Iran
b
Department of Pharmacognosy, Medical University of Bialystok, Mickiewicza 2a, 15-089, Bialystok, Poland
c
Department of Experimental, Diagnostic and Specialty Medicine-DIMES, General Pathology Unit, Alma Mater Studiorum, University of Bologna, Via San Giacomo 14,
40126, Bologna, Italy
d
Laboratory of Microbiology and Molecular Biology, Department of Biological Chemistry, Universidade Regional do Cariri – URCA, Crato, CE, Brazil
e
Medical Ethics and Law Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
f
Student Research Committee, Shahid Beheshti University of Medical Sciences, Tehran, Iran
g
Centro Interdipartimentale di Ricerca Industriale Agroalimentare, Università degli Studi di Bologna, Cesena, Italy
h
Departamento de Ingeniería Química, Ambiental y de los Materiales, Universidad de Jaén, Spain
i
Department of Botany, Lahore College for Women University, Jail Road Lahore, Pakistan
j
Department of Chemistry, University of Alabama in Huntsville, Huntsville, AL, 35899, USA
k
Department of Botany & Postgraduate Department, Biological Sciences, VIVA College of Arts, Science & Commerce, Virar (w), 401303, Maharashtra, India
l
Department of Nutrition and Dietetics, Faculty of Pharmacy, University of Concepcion, Concepcion, Chile
m
Research Group on Community Nutrition and Oxidative Stress, Laboratory of Physical Activity Sciences, and CIBEROBN – Physiopathology of Obesity and Nutrition,
CB12/03/30038, University of Balearic Islands, Palma de Mallorca, Spain
n
Phytochemistry Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
o
Department of Chemistry, Richardson College for the Environmental Science Complex, The University of Winnipeg, Winnipeg, Canada

A R T I C LE I N FO A B S T R A C T

Keywords: Matricaria is a widespread genus of flowering plants of the family Asteraceae that grow in temperate regions of
Antimicrobial compounds Europe, Asia, America and Africa. Some of the species are also naturalized in Australia. Some species of this
Chamomiles genus such as Chamomiles are recognized medicinal plants and cultivated in several countries for commercial
Essential oil purposes: to obtain its blue essence, as herbal tea, and for pharmaceutical or cosmeceutical uses. The phyto-
Natural food preservative
chemical composition of Matricaria spp. includes volatile terpenoids (e.g., α-bisabolol, bisabolol oxide A and B,
Matricaria
β-trans-farnesene and chamazulene), sesquiterpene lactones such as matricin, and phenolic compounds (flavo-
Matricaria recutita
noids, coumarins and phenolic acids). Their essential oil is obtained from the fresh or dried inflorescences by
steam distillation, and additionally cohobation of the remaining water. The volatile composition of the essential
oil, especially the content of the valuable components α-bisabolol and chamazulene, depends on the plant part,
origin and quality of the source, genetic, and environmental factors. Moreover, other parameters, such as season
of harvest and methods of extraction, can affect the extraction yield of the essential oils/extracts, their com-
position and, therefore, their bioactivity. Due to the importance of this genus and particularly M. recutita (M.
chamomilla), this review focus on its cultivation, factor affecting essential oils’ composition and their role in
traditional medicine, as antibacterial agents and finally as food preservatives.


Corresponding author at: Phytochemistry Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran and Department of Chemistry, Richardson College for the
Environmental Science Complex, The University of Winnipeg, Winnipeg, Canada.
⁎⁎
Corresponding author at: Medical Ethics and Law Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran and Student Research Committee, Shahid Beheshti
University of Medical Sciences, Tehran, Iran.
⁎⁎⁎
Corresponding author at: Department of Nutrition and Dietetics, Faculty of Pharmacy, University of Concepcion, Concepcion, Chile.
E-mail addresses: bahar.salehi@sbmu.ac.ir, bahar.salehi007@gmail.com (B. Salehi), mmartorell@udec.cl (M. Martorell),
javad.sharifirad@sbmu.ac.ir, javad.sharifirad@gmail.com (J. Sharifi-Rad).

https://doi.org/10.1016/j.micres.2018.06.010
Received 1 June 2017; Received in revised form 5 June 2018; Accepted 23 June 2018
Available online 25 June 2018
0944-5013/ © 2018 Elsevier GmbH. All rights reserved.
M. Sharifi-Rad et al. Microbiological Research 215 (2018) 76–88

1. Introduction According to most of reports, the ideal temperature to dry the


flowers is 35–38 °C and the necessary time to do this is 36–72 h.
Matricaria is a genus of flowering plants and falls under the same Alternatively, this temperature in electric driers is 40–60 °C. By manual
family as common species such as sunflower (Helianthus annuus), let- harvesting, production of fresh flowers is 2 tons per hectare. This re-
tuce (Lactuca sativa), and artichoke (Cynara scolymus), i.e., Asteraceae. sulted in 100–500 kg dried product. In mechanized harvest, 400–800 kg
Most of the species of this genus are commonly found in temperate hectare flowering stem would be collected to produce the essence. Early
regions of Europe, Asia and America, and also in northern and southern or late harvest would bring about quality reduction of effective mate-
Africa (Bremer and Humphries, 1993; Singh et al., 2011; Miraj and rials. The flowers have maximum amounts of essence when ray florets
Alesaeidi, 2016). Some of the species are naturalized in Australia. They are fully bloomed. The flowers should be dried immediately after the
are annual aromatic herbs that can be found growing on lands rich in harvesting. Any delay can bring changes in flowers color and reduction
nutrients as well as on roadside. of their essence quantity (Anderson et al., 1996; Fontanarosa, 2000).
These genus are much branched and these many branched stems are While somewhere in India this crop is of 4–6 months and propa-
prostrate to erect, glabrous, and leafy (Bremer and Humphries, 1993; gated by seeds either by transplanting or direct sowing. Since it is a
Singh et al., 2011). Flowers are radially symmetrical, heads solitary, Rabi crop it is sown on second fortnight of December in North Indian
either heterogamous with white ray florets female flowers (M. recutita, hills, while in plains it is sown in late September. Crop requires
also known as M. chamomilla) or homogamous and lacking ray florets 20–25 tons of farmyard manure (Nidagundi and Hegde, 2007). Flowers
(M. discoidea). The leaves are 2–3 pinnatisect and repeatedly divided can be used fresh, frozen or dried. Harvesting is best during tempera-
into segments which are narrowly linear. Receptacle is conical, hollow tures of 22–25 °C.
and lacks receptacular scales. Achenes are obovoid and somewhat lat-
erally flattened, obliquely truncate above, inconspicuously 3–5 ribbed 3. Chemical composition of essential oils obtained from genus
on the posterior face and without oil glands on the anterior side. The Matricaria plants
pappus may be crown shaped and short or lacking.
Genus Matricaria comprises plants with various secondary metabo- The essential oil is characteristic for some genera from the
lites of varied chemical nature. A number of chemical components have Asteraceae family, including the Matricaria genus, as commented be-
been isolated from genus Matricaria (Kazemi, 2014). A majority of the fore. Among species from this genus, the most popular and commer-
chemical constituents have been recorded mainly in Matricaria chamo- cially important is M. recutita (Baser and Buchbauer, 2015). The es-
milla also called as German chamomile. Plants belonging to this genus sential oil is found in the whole plant (Das et al., 2002), but the flower
have shown the presence of components like volatile compounds, ses- head is mostly used for medicinal and aromatic purposes. Volatile
quiterpene lactones, and phenolic compounds such as flavonoids (fla- compounds and sesquiterpene lactones are secreted to the multicellular
vones and flavonols) and coumarins (Table 1). biseriate glandular hairs and to the glandular ducts localized mostly on
some parts of flowers—the former on the bract, corolla, ovary and the
2. Cultivation of plants from the genus Matricaria latter in the inflorescence peduncle, receptacle, bract, and stigma. Both
secretory structures are present on stems and leaves but in considerably
The chamomile genus Matricaria is one of the most important and smaller amount (Andreucci et al., 2008). The monograph of Matricariae
well-known herbal drugs. Chamomiles are grown commercially in flos (M. recutita flower) is placed in many national pharmacopoeias and
Europe, North Caucasus to South Siberia, the intercontinental state European Pharmacopoeia (EP) which recommend that chamomile
Turkey, Asia (Afghanistan, Pakistan, North India, and Japan), North contains no less than 4 mL/kg of blue essential oil (Schilcher, 2005). In
Africa (Egypt, Ethiopia), North and South America (east coast of the addition, Matricariae aetheroleum (M. recutita oil) also has its mono-
USA, Cuba, Argentina, and Brazil) and New Zealand (Singh et al., graph in EP, in which two types of oil are mentioned—rich in bisabolol
2011). It is cultivated mostly for its blue essence, as herbal tea, and in oxides (29–81%) and rich in levomenol (10–65%) (European
view of its ever-increasing usage in pharmaceutical, cosmetic and sa- Directorate for the Quality of Medicines and Healthcare, 2004).
nitary, perfumery industry, and production of nutritional flavors The essential oil is obtained from the fresh or dried inflorescences
(Mohammad, 2011). This important medicinal plant has been culti- by steam distillation. Sometimes this process is long-drawn (even
vated from two chamomiles: Roman chamomile, Chamamelum nobile L., 7–13 h) and additionally cohobation of remaining water is being carried
with ancient name Antemis nobilis and German chamomile, Matricaria out. The yield of the process is around 0.3–1.5% and depends on origin
recutita (M. chamomilla). and quality of the source. This is a deep blue, viscous liquid with an
German chamomile requires cool, temperate conditions to grow intense characteristic herbaceous odor (Schilcher, 1987; Sticher, 2010).
well, with temperature ranging from 7 to 26 °C. German chamomile can There is a big diversification in qualitative and quantitative com-
survive cold winter nights as low as −12 °C (Singh et al., 2011). Al- position of volatile fractions obtained from the plant materials from
though chamomile is drought tolerant, it needs enough water to ger- various countries and regions of origin. Nevertheless, the primary
minate and for the development of the young plants. German chamo- constituents are sesquiterpenes such as (-)-α-bisabolol (levomenol,
mile requires no extra water once properly established. An annual 5–70%), bisabolol oxide A (5–60%), bisabolol oxide B (5–60%), bisa-
precipitation of 400 to 1400 mm per season is enough to produce a bolone oxide (0–8%), (E)-β-farnesene (7–45%), chamazulene (1–35%),
good crop. German chamomile can be grown on a wide range of soil and polyacetylenic compounds named spiroethers, existing in two iso-
types, but prefers a well-drained, sandy or sandy-loam soil with a pH of meric forms, trans-(Z)- and cis-(E)-en-yne-dicycloether (2–30%).
4–8 grows in any other soils that have good drainage. Each plant nor- Monoterpenes like limonene (0.1%), (Z)-β-ocimene (0.69%), γ-terpi-
mally produces from 12 to 14 sets of runners. Make sure plants with nene (0.17%) and artemisia ketone (0.32%) were also detected (Wichtl,
superior qualities are used for vegetative propagation. Spacing of plants 2004; Heuskin et al., 2009). Fig. 1 presents the most abundant com-
should be 30 × 30 cm (Dutta and Singh, 1964). German chamomile pounds of chamomile essential oil.
does not require large quantities of fertilizers, but depending on soil Tirillini et al. (2006) have identified the largest number of compo-
tests, small quantities of nitrogen, phosphorus, and potassium should be nents of Matricaria essential oil. They analyzed separate elements of
applied before planting. Sprinkler irrigation should be used. Constant flower heads—ligulate and tubular florets and receptacle from plants
weeding is necessary until the chamomile ‘mat’ takes over. Whiteflies, growing in Italy. In all cases, more than 70 compounds were identified
aphids, spider mites, and thrips are the major insect pests affecting representing about 99% of the components of the oils. The oxygenated
chamomile. Flower heads are harvested in the summer while in full sesquiterpenoids and sesquiterpene hydrocarbons were predominating
bloom (Bremer and Humphries, 1993; Singh et al., 2011). in essential oil from tubular florets obtained with a yield of 0.95%, the

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M. Sharifi-Rad et al. Microbiological Research 215 (2018) 76–88

Table 1
Chemical compounds reported in Matricaria spp.
Compound Source Reference

Bisabolene M. chamomilla (Orav et al., 2001)


β-Caryophyllene M. chamomilla (Reichling et al., 1983)
α–Pinene M. chamomilla (Pirzad et al., 2006)
β-elemene M. chamomilla (Pirzad et al., 2006)
α–Terpinene M. chamomilla (Pirzad et al., 2006)
1,2, 3,6,7-pentahydroxy- bisabolol-10(11)-ene M. aurea (Ahmed and Elela, 1999)
1,2, 3,6,7-tetrahydroxy-1- acetoxy-bisabolol- M. aurea (Ahmed et al., 1993)
10(11)-ene
1,2, 3,6,7-tetrahydroxy-2- acetoxy-bisabolol- M. aurea (Ahmed and Elela, 1999)
10(11)-ene
1,6,7- trihydroxy-1- acetoxybisabolol-2,10- diene M. aurea (Ahmed et al., 1993)
1,6,7- trihydroxy-bisabolol-2,10-diene M. aurea (Ahmed et al., 1993)
3,4- dihydroxy-2 (hexa-2,4 diynyliden)-1,6-dioxaspiro-(4,5) decane M. aurea (Ahmed and Elela, 1999)
Anisic acid M. chamomilla (Reichling et al., 1979)
Apigenin M. chamomilla (Power and Browning, 1914; Sorm et al., 1951; Kunde and Isaac, 1979)
Apigenin-7-(6″-O- acetyl)-glucoside M. chamomilla (Kunde and Isaac, 1979)
Apigenin-7-(6″-O-apiosyl)-glucoside (apiin) M. chamomilla (Wagner and Kirmayer, 1957; Kunde and Isaac, 1979)
Apigenin-7-glucoside (apigetrin) M. chamomilla (Lang and Schwandt, 1957; Hörhammer et al., 1963; Kunde and Isaac, 1979)
Bicyclogermacrene M. chamomilla (Pirzad et al., 2006)
Bisabolol M. chamomilla (Sorm et al., 1951)
Bisabolol oxide A M. chamomilla (Sampath et al., 1969)
Bisabolol oxide B M. chamomilla (Sampath et al., 1969)
Bisabolol oxide C M. chamomilla (Schilcher et al., 1976)
Bisabolone oxide M. chamomilla (Pirzad et al., 2006)
Cadinene M. chamomilla (Shams-Ardakani et al., 2006)
Caffeic acid M. chamomilla (Reichling et al., 1979)
Calamemene M. chamomilla (Motl and Repcak, 1979)
Caryophyllene epoxide M. chamomilla (Reichling et al., 1983)
Chamavioline M. chamomilla (Motl and Repcak, 1979; Motl et al., 1983)
Chamazulene M. chamomilla (Ness et al., 1996)
Chamazulene carboxylic acid M. chamomilla (Stahl, 1954)
Chrysoeriol M. chamomilla (Reichling et al., 1979)
Chrysoeriol-7-glucoside M. chamomilla (Greger, 1975)
Chrysosplenitin M. chamomilla (Hänsel et al., 1966)
Chrysosplenol M. chamomilla (Hänsel et al., 1966; Exner et al., 1981)
Esculetin M. chamomilla (Kotov et al., 1991)
Eupatilin M. chamomilla (Hänsel et al., 1966; Exner et al., 1981)
Eupatoletin M. chamomilla (Hänsel et al., 1966; Kunde and Isaac, 1979; Exner et al., 1981)
Gerianol M. chamomilla (Stransky et al., 1981)
Germacrene A M. chamomilla (Pirzad et al., 2006)
Germacrene D M. chamomilla (Pirzad et al., 2006)
Herniarin M. chamomilla (Schilcher, 1985)
Isoscopoletin M. chamomilla (Kotov et al., 1991)
Luteolin M. chamomilla (Kunde and Isaac, 1979)
Luteolin-4′-glucoside M. chamomilla (Greger, 1975; Kunde and Isaac, 1979)
Luteolin-7-glucoside M. chamomilla (Greger, 1975; Kunde and Isaac, 1979)
Lutuletin M. chamomilla (Kunde and Isaac, 1979)
Matricarin M. chamomilla (Čekan et al., 1959)
Matricin (proazulene) M. chamomilla (Sorm et al., 1951; Čekan et al., 1957)
Muurolene M. chamomilla (Motl and Repcak, 1979)
Myrcene M. chamomilla (Stransky et al., 1981)
Quercetin M. chamomilla (Greger, 1975; Kunde and Isaac, 1979)
Quercetin-7-glucoside (quercimeritrin) M. chamomilla (Lang and Schwandt, 1957; Kunde and Isaac, 1979)
Sabinene M. chamomilla (Pirzad et al., 2006)
Scopoletin M. chamomilla (Kotov et al., 1991)
Spathulenol M. chamomilla (Motl et al., 1977)
Synergic acid M. chamomilla (Reichling et al., 1979)
Umbelliferone M. chamomilla (Schilcher, 1985)
Vanillic acid M. chamomilla (Reichling et al., 1979)

sesquiterpene hydrocarbons in ligular florets (a yield of 0.70%) and the chamomile (M. recutita) flower-heads using the chemical characterizing
oxygenated sesquiterpenoids and sesquiterpene hydrocarbons in re- components defined by Schilcher (1987) and determined by (A) con-
ceptacle (a yield of 0.75%). ventional gas chromatography (GC) analysis and (B) headspace–solid-
According to the content of the main components, within the species phase microextraction fast GC (HS-SPME F-GC). These analyses can be
the following six chemotypes are distinguished: type A (bisabolol oxide useful for standardizing an average composition of chamomile che-
A as main component), type B (bisabolol oxide B as main component), motypes, since the groups could be clustered adequately, but with a
type C (α-bisabolol as main component), type D (comparable amounts partial overlapping of the chemotypes type C and D.
of α-bisabolol and bisabolol oxide A and B), another types characterized In Europe, several diploid and tetraploid German chamomile culti-
by α-bisabolone oxide A as main component or the green essential oil vars are growing with different plant characteristics and quality para-
with low amount of matricin in source (Schilcher, 1987). In this regard, meters (Honermeier et al., 2013). It was observed that these genotypes
Fig. 2 shows a principal component analysis (PCA) of 92 essential oils of growing in Serbia differed in the content and composition of essential

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Fig. 3. The conversion of matricin during the process of hydrodistillation.

not detected (Kazemi, 2014).


In the case of α-bisabolol, its concentration in the plant is dependent
on genetic, ontogenetic and environmental factors (Ghasemi et al.,
Fig. 1. The main components of M. recutita essential oil. 2016). Malta and Crimea are places where the content of bisabolol in M.
recutita oil is very high, 67 and 69%, respectively (Salamon, 2009). A
high concentration (over 40%) was found also in Moldavian and
oil. Additionally, the differences were detected in tubular and ligulate
Hungarian oils (Gosztola et al., 2010; Orav et al., 2010).
florets of these two forms; the first type contained about two times more
M. recutita is a very important medicinal plant and, consequently,
of volatile fraction than the second. Moreover, since the ratio of tubular
producers introduce new cultivars into cultivation, which help to
and ligulate florets is 9:1 (w/w), the main part of essential oil derives
supply large amounts of plant material of high quality for pharma-
from tubular florets. In tubular and ligulate florets of diploid, α-bisa-
ceutical purposes (Seidler-Lozykowska, 2006; Shalaby et al., 2010). In
bolol, α-bisabolol oxide A and α-bisabolol oxide B were predominating,
Slovakia, thanks to selection, a diploid cultivar with high concentration
while in both types of the florets of tetraploid, α-bisabolol oxide A was
of α-bisabolol and chamazulene, more than 55 and 16%, respectively
the main component (Pekic et al., 1999).
was received (Fejer and Salamon, 2014). Chief producers of German
α-Bisabolol and chamazulene are considered to be the most valuable
chamomile essential oil are Argentina, Egypt, and Hungary (Lawless,
components of essential oil. Chamazulene is an artifact, which forms
2013).
from the colourless, non-volatile sesquiterpene lactone matricin by
There are a few publications concerning the composition of essential
deacetylation, dehydratation and decarboxylation in the process of
oil from another species of the genus Matricaria. In the oil from the
distillation (Fig. 3) (Wichtl, 2004). Its concentration is different in oils
flower heads of M. aurea (Loefl.) Sch. Bip growing in Saudi Arabia, the
from various regions of the world. Essential oil obtained from Matricaria
predominating component is bisabolol oxide A (65%) (Siddiqui, 2014).
flos growing in Armenia and Poland contained more than 15% of cha-
In a volatile fraction obtained by simultaneous distillation/extraction
mazulene (Orav et al., 2010). Data from Poland additionally suggested
method from M. matricarioides (Less.) Port. (syn. M. discoidea, M. sua-
that the cultivated plants (tetraploid cultivare ‘Złoty Łan’) contained
veolens (Pursh) Buch.) fresh and dried herb, 24 components were
higher concentration of this compound than the wild-growing: 25% and
identified representing more than 95% of total. In this colourless oil, the
16%, respectively (Nurzyñska-Wierdak, 2011). Contrastively, in oils
major compounds were myrcene (26%), (E)-β-farnesene (16%), geranyl
from, e.g., Egypt, India, Greece, Germany or England the content of
isovalerate (13%) and en-yne-dicycloethers (35%) (values for dried
chamazulene was less than 2% (Das et al., 2002; Orav et al., 2010;
plant material). Moreover, quantitative differences were observed be-
Singh et al., 2011), whereas in Iranian essential oil this compound was
tween the fresh and dried plant oils, particularly in the amounts of

Fig. 2. PCA scatter plot of chamomile essential oils of chamomile flower-heads using the main chemotypes (A or a, B or b, C or c and D or d) defined by Schilcher
(1987). The analyses were performed by A) conventional GC and B) HS-SPME F-GC. Adapted from (Rubiolo et al., 2006) with permission of John Wiley & Sons
(2017).

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myrcene and (E)-β-farnesene. α-Bisabolol oxide B, bisabolone oxide A, chamomile (Bostock, 1855). He also wrote that all parts of the plant
α-bisabolol and chamazulene were present but in low amounts (Orav were utilized as an antidote against snake bites. Moreover, chamomile
et al., 1999). Similar qualitative composition was found in the oil from was utilized as diuretic and to dissolve bladder calculi, for the treat-
Canada. Certain differences were detected in quantity of particular ment of flatulence and for affections of the liver. Another use reported
components (Lopes and Kolodziejczyk, 2005). Boutaghane et al. (2011) by Pliny the Elder was the local application for the treatment of fistulas
investigated aerial parts of M. pubescens (Desf.) Schultz. growing in of the eye. Additionally, the topical application of the pulverized plant
Algeria, which comprised 1% yellowish essential oil. Among 39 iden- was used to treat suppurating sores. Pliny reported that given as a
tified compounds, representing 92% of total oil, isochrysanthemic acid drink, the plant was emmenagogue and can be useful to expel a dead
ethyl ester (27%), spathulenol (19%), α-cadinol (13%) and geranyl fetus. Amongst Roman physicians, and subsequently amongst Arabian
isovalerate (8%) were predominating. In the whole plant of M. songarica physicians, chamomiles were considered a plant that had strong abor-
from China, in total 55 compounds (representing 0.64% of plant) were tive action and could accelerate menstruation and embryo release.
identified in the essential oil. Among the components, (E)-β-farnesene In the Middle Ages, chamomile was highly considered in monastic
(11%), bisabolol oxide A (11%), α-bisabolol (9%), (Z,Z)-matricaria ester medicine. Chamomile was recommended for pains of the stomach and
(8%), (E,E)-farnesol (8%), (E,Z)-matricaria ester (4%) were stated as the abdomen, for dermatitis, for menstrual troubles, as gargling for in-
predominant compounds (Jian-Yu et al., 2012). flammations of the mouth, as baths for inflammation in genital area
It is very difficult to state what exactly the composition of the es- (Srivastava and Gupta, 2011). Charlemagne, king of the Franks and
sential oil of Matricariae flos is because a large variation is observed not Christian emperor of the West, in the Capitulare de villis, a guide for the
only between oils from different countries, but also between those from governance of the royal estates, inserted chamomile amongst the plants
the regions of one country. Taking this into consideration, it is very he wanted cultivated on his properties (Waggoner, 2011). In that period
important to use standardized substances for medicinal purposes. chamomile was considered one of the most-respected plants. Christians
consecrated chamomile to St. Anne, mother of the Virgin. The pagan
4. The genus Matricaria in traditional medicine Anglo-Saxons considered chamomile one of the ‘Nine Sacred Herbs’
given to the humankind by the Nordic god Woden (Gordon, 1962).
Historically, Roman (Chamaemelum nobile) and German (M. recutita) The Arabs absorbed the Ancient Greek and Roman knowledge about
chamomiles have been often used interchangeably or confused. The the therapeutic use of chamomile. In the Islamic Golden Age, the
term “chamomile” comes from a Greek word meaning "ground apple" Persian physician Avicenna (980–1037 AD), who was the author of the
which refers to the smell of chamomile that resembles that of some famous book Canon of Medicine, represented the starting point of Unani
varieties of apple. This derivation is preserved in the Spanish name medicine. This traditional system of healing and health maintenance
“manzanilla”, from “manzana”, which means “apple”. The name persisted for many centuries in all areas of Islamic culture. In the Canon
“Matricaria” originates from the Latin (matrix means uterus), the term of Medicine, Avicenna suggested the efficacy of some medicinal herbs,
derives from its application in women as a phytotherapeutic for pro- and amongst them is chamomile, used by him for headache treatments,
blems associated with the menstrual cycle and abortus. edema, conjunctivitis, jaundice, chronic fever, lithiasis, amenorrhea,
The first written report of chamomile is in the Ancient Egypt. “Ebers toothache, aphthous ulcers and muscle tightness. Chamomile was also
Papyrus” represents the first written collection of plant usage (con- recommended to relieve itching and inflammation and facilitate healing
taining over 800 recipes) for medical purposes in Ancient Egypt. It is a of skin lesions in patients undergone surgeries (Mahdizadeh et al.,
medical papyrus dating back to about 1500 BCE, although it is probably 2015).
a reedition of much older receipts. In the papyrus, an important role All these ancient manuscripts strongly influenced the medical
was given to Matricaria (Ebers, 1987). Chamomile crushed flowers thinking of Mediterranean physicians until the development of modern
were used to give skin relief and to prevent dermatitis and for cosmetic medicine. However, plant-based remedies have survived until today
preparations. Ancient Egyptians used this plant not only to cure the sick with the oral traditions passed on by local folk medicines and are now
but also to honor the gods and embalm the dead. In the Ramses II having a new Renaissance. The analgesic and anti-inflammatory effects
mummy bandages, traces of pollen from Matricaria were found; this of chamomile have been largely proved by current medicine, see for
plant probably was included in order to give the Pharaoh the strength example (Shoara et al., 2015). Chamomile was absent in the original
and calm needed for the afterlife journey (Cattabiani, 1996). ancient Chinese Traditional Medicine and Ayurveda, but it has been
Egyptian information about herbal medicine and drug preparation introduced more recently.
provided the base for the Greek and Roman pharmacopoeias.
Hippocrates of Kos (5th century BC), universally recognized as the fa- 5. Ethnobiology of the Matricaria genus related to bacterial
ther of modern medicine, had deep knowledge of medicinal herbs. infections
Hippocrates recommended chamomile for therapeutic use in several
diseases, such as for purification, protection and to fight colds. Species from the Matricaria genus are widely used in Europe, Latin
Asclepiades of Bithynia (1st century BC) was the first physician to es- America, Asia and Africa to treat signs and symptoms related to bac-
tablish Greek Medicine in Rome. He was a great expert in plant for terial infections. Generally, the aerial parts are used, especially the
medical use and his favorite herb was chamomile (Gumpert, 1794). flowers, although the use of the whole plant has also been mentioned
Dioscorides (1st century AD) was a military physician and pharma- (Miraj and Alesaeidi, 2016). For the treatment of gastrointestinal and
cognosist of Nero’s Army. Many chamomile (Anthemis arvensis, corn urinary disorders the main form of administration is oral, where teas
chamomile) applications were described in his work De materia medica. are prepared in the form of decoction or infusion. However, for pro-
Some examples from De materia medica are: roots, flowers or herb, blems related to the respiratory system, in addition to the oral use,
taken as decoction, were reported to be useful as a tonic, for cleansing inhalation is also indicated, while topical applications are cited to treat
and rinsing the eyes, ears, nose, and mouth. Such decoctions were also skin disorders. Although the genus has medicinal versatility, its use for
useful to expel urinary stones and gallstones, for gastro-intestinal dis- the treatment of gastrointestinal disorders stands out above all others
orders (to treat worms, peptic ulcers, spasms and inflammation), for (Table 2). In the ethnomedicinal context, from the species used to treat
jaundice and liver ailments. Topical applications of the plant were used diseases, M. occidentalis Greene and M. recutita, are the most cited in
as an antiphlogistic to cure wounds, stings, burns, and ulcers. Suppo- literature, followed by M. discoidea DC., M. aurea (Loefl) Sch. Bip. and
sitories of chamomile were advised for recurrent fevers (Osbaldeston M. frigidum (HBK) Kunth, with the latter having its medicinal use re-
and Wood, 2000). Pliny the Elder, who was contemporary of Dioscor- ported only in Peru (Bussmann et al., 2007).
ides, in his work Naturalis Historia described many application for Concerning scientific literature, several biological activities such as

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M. Sharifi-Rad et al.

Table 2
Use of Matricaria genus in folk medicine against signs and symptoms related to bacterial infection.
Species Indication Used part Ways to use Preparation administration Reference Country

Matricaria aurea (Loefl.) Digestive system disorders (spasms, Aerial parts; Infusion, Internal and external use – oral, (Ali-Shtayeh et al., 2000; Aburjai et al., Iran, Lebanon, Jordan, Palestine,
Sch. Bip. intestinal gas, diarrhea, stomach and whole plant decoction, tea drenched, boiled, 2007; Nawash et al., 2013; Arnold et al.,
abdominal pain), respiratory disturbances vaporization. 2015; Moein et al., 2015; Oran and Al-
(cough, sore throat), infection, skin Eisawi, 2015)
disorders.
Matricaria chamomilla L. Gastrointestinal diseases (astralgia, digestive Aerial parts; Infusion, Oral use: two teaspoons of dried flower (Ballero et al., 2001; Jarić et al., 2007; Italy, Spain, Kosovo, Pakistan, Slovenia,
disorder, dysentery and diarrhea, abdominal whole plant decoction, tea, per cup of tea, steeped for 10 to Maxia et al., 2008; Vitalini et al., 2009; Iran, Turkey, Bulgaria, Romania, Jordan,
pain, flatulence, constipation, intestinal maceration. 15 minutes while covered to avoid Benítez et al., 2010; Gómez-Estrada et al., Algeria, Serbia, Bolivia, Brazil,
colic, stomach pain, dyspepsia, spasms), evaporation of volatile oils; Cooked in 2011; Sekkoum et al., 2011; Angulo et al., Romania, Colombia, Palestine.
respiratory tract diseases (sinusitis, rice 2012; Mustafa et al., 2012; Quiroga et al.,
pharyngitis, sore throat, bronchitis, cough), Oral use - Drink one teacup (aerial 2012; Gürdal and Kültür, 2013; Jaradat
genital infection, urolithiasis and urinary parts) 2–3 times a day for 2–3 days; and Adawi, 2013; Kozuharova et al.,
tract infections, eye infection drink one-two tea cups in case of need/ 2013; Sargın et al., 2013; Šavikin et al.,
(conjunctivitis), fever, bactericidal, earache, before go to bed (antispasmodic) 2013; Ajaib et al., 2014; Tahvilian et al.,
wounds and skin ulcers, skin infection, face Internally/inhalation (anthodium 2014; Al-Quran et al., 2015; Pieroni et al.,
disinfection decoction) 2015; Ahmed, 2016; da Costa et al., 2017;
Oral use: fresh, soaked. Cool and oral Lumpert and Kreft, 2017)

81
taken whenever needed.
Topical use: put the mixture on a cloth
and insert in the ear (earache); direct
external applications, or in tea or in
oleolite (wounds and skin ulcers),
dressing.
Matricaria Gastrointestinal system disorders Flowers Balm, tea Oral use; external use (Saric-Kundalic et al., 2010) Bosnia and Herzegovina
discoidea DC. (flatulence; stomachache), wounds, ulcers,
throat inflammations
Matricaria frigidum Colic, stomach ache, bronchitis Not Not informed Not informed (Bussmann et al., 2007) Peru
(H.B.K.) Kunth informed
Matricaria pubescens - Digestive diseases (gastric ulcer, stomach Whole plant Maceration Oral use (Djellouli et al., 2013; Ramdane et al., Algeria
synonym of pain, abdominal pain, constipation), Decoction, Inhalation 2015; Lakhdari et al., 2016)
Matricaria problems of respiratory system (cough), Infusion, powder
occidentalis Greene rheumatism, fever.
Matricaria recutita L. - Gastrointestinal system disorders (acute Whole plant Tea, decoction, Oral use: 2 cups boiling water 2-3 Germany, Egypt, Brazil, Czech Republic,
synonym of gastroenteritis, spasms, stomach diseases, Aerial parts infusion, powder tablespoons flowers by infusing (in Ecuador, Bosnia and Herzegovina,
Matricaria gastrointestinal tract gastritis, peptic ulcer, Thermos), should be taken 3 times a Mexico, Croatia, Argentina, Ecuador,
occidentalis Greene abdominal pains, indigestion, intestinal day. Bolivia, Italy, Croatia, Serbia, Portugal,
constipation, colon colic, diarrhea, nausea/ Boil about a cup of water and add a Azerbaijan, Switzerland, German,
vomiting, flatulence), respiratory system handful of manzanilla flowers. Mexico/United States of America,
disorders (cough, sore throat, bronchial Used in very hot infusions. Navarra, Spain, Bolivia, Peru
diseases), urinary tract infections, skin Topical use: cleaning wounds, gargles
disorders (wounds, acne), conjunctivitis, .
toothaches, oral biofilm control, infection,
fever.
(continued on next page)
Microbiological Research 215 (2018) 76–88
M. Sharifi-Rad et al.

Table 2 (continued)

Species Indication Used part Ways to use Preparation administration Reference Country

(Bonet et al., 1999; Fernandez et al., 2003;


Hernández et al., 2003; Pieroni et al.,
2003; De Souza et al., 2004; Novais et al.,
2004; Macía et al., 2005; Waldstein, 2006;
Akerreta et al., 2007; Redžić, 2007;
Pieroni and Giusti, 2008; Pieroni and
Gray, 2008; Jeschke et al., 2009; Parada
et al., 2009; Idolo et al., 2010; AbouZid
and Mohamed, 2011; Huamantupa et al.,
2011; Pieroni et al., 2011; Pochettino
et al., 2011; Alonso-Castro et al., 2012;
Schmid et al., 2012; del Carmen Juárez-
Vázquez et al., 2013; Jerves-Andrade
et al., 2014; Baliano et al., 2015; De David
and Pasa, 2015; Ibadullayeva, 2015;
Vlková et al., 2015; Nascimiento et al.,
2016; Tinitana et al., 2016)

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M. Sharifi-Rad et al. Microbiological Research 215 (2018) 76–88

anti-inflammatory, antimicrobial, antispasmodic, analgesic among extracts presented antibacterial activity against S. aureus and E. coli.
others, are attributed to plants of the Matricaria genus (Singh et al., The ethanolic extract showed an inhibition zone of 14 mm and 16 mm
2011; Miraj and Alesaeidi, 2016), although, in this review, we have for E. coli and S. aureus, respectively, and the methanolic extract one of
focused in its antibacterial activity. Most researches are often directed 12 mm for E. coli and 14 cm for S. aureus. Thus, the plant tested has a
through ethnobiological approaches, although random and chemo- higher antibacterial percentage against the Gram-positive strain S.
taxonomic approaches are also used as selection strategies for research aureus. This can be explained by the fact that there is a greater com-
objects (Albuquerque and Hanazaki, 2006). Potentially active chemical plexity of the double layer that surrounds Gram-negative bacteria,
constituents of M. recutita include terpenoids and spiroethers, flavo- causing the natural products to have a reduced activity in them, when
noids and coumarins, which are believed to be responsible in part for compared to Gram-positive organisms. The oils also exerted better an-
such a wide range of biological activities (Barnes et al., 2003). Extracts tibacterial activity against Gram-positive bacteria in comparison to
of chamomile flowers can be used as a rich source of phenolic com- Gram-negative bacteria, although the mechanism of action has not been
pounds, among which apigenin is recognized as one of the most elucidated yet. In the methodology employed in this study (Munir et al.,
bioactive compounds (Cvetanović et al., 2015b). 2014), the oils have a lower water solubility, thus presenting lower
Kazemi (2014) studied the phytochemical profile of some Matricaria values when compared with the microdilution methodology. Using the
species essential oils by gas chromatography–mass spectrometry. This same methodology, Mekonnen et al. (2016) evaluated the in vitro an-
author showed different antimicrobial activities of these oils against timicrobial activity of the M. recutita essential oil against Salmonella
both Gram-positive and Gram-negative bacteria, suggesting a biological paratyphi, Salmonella typhimurium, Shigella spp., P. aeruginosa, S. aureus
activity correlated to the chemical composition of the oils. Pauli (2006) and E. coli. The part used for extracting the oil was the chamomile
reported that α-bisabolol may inhibit fungal growth via specific in- flower and was unable to inhibit any bacterial growth, which can be
hibition of ergosterol biosynthesis. Marino et al. (2001) tested a wide explained by the low α-bisabolol concentration (4%), the component
range of essential oils for their inhibitory effects against nine strains of responsible for the antimicrobial activity. This low value may be as-
Gram-negative bacteria and six strains of Gram-positive bacteria, sociated with the seasonality and altitude at which the plant was col-
showing that Matricaria essential oils had generally a bacteriostatic lected.
activity, especially against Gram-positive bacteria (e.g., Listeria in- Fabri et al. (2011) investigated the antimicrobial and antioxidant
nocua). However, many parameters, such as season of harvest and potential of several plant species, all belonging to the Asteraceae fa-
methods of extraction, can affect essential oil extraction yield, their mily, among them M. recutita. The methanolic extract from chamomile
composition and, therefore, their antimicrobial activities (Hyldgaard leaves was tested by the broth microdilution technique against S.
et al., 2012; Calo et al., 2015). The effects of different solvents (with aureus, P. aeruginosa, S. enterica serovar typhimurium, Shigella sonnei,
different polarities) and different extraction techniques on the chemical Klebsiella pneumoniae, E. coli and Bacillus cereus. The results were
composition and biological activities of chamomile extract have been compared with the positive control that was chlorofenicol. M. chamo-
studied, showing that these parameters can deeply modify Matricaria milla presented a MIC of 78 μg/mL for P. aeruginosa, proving to be ef-
spp. oil/extract composition and the minimum inhibitory concentration ficient, while the chlorofenicol control still showed a better result, a
(MIC) against several pathogen strains (Cvetanović et al., 2015a; MIC of 15 μg/mL. In addition, the authors of this study performed the
Metrouh-Amir et al., 2015). In particular, the latter authors found that chemical prospection of the extract, detecting the presence of tri-
M. recutita subcritical water extracts showed the highest activity against terpenoids, phenols, tannins, flavonoids, suggesting that these compo-
Escherichia coli and Aspergillus niger with a MIC of 39 μg/mL. nents may be responsible for the observed antimicrobial activity.
The methodology recommended by the National Committee for Carvalho et al. (2014) studied the antibacterial activity of the ethanolic
Clinical Laboratory Standards (NCCLS) (Patel et al., 2012) for anti- extract and the cyclohexane extract obtained from commercially pur-
bacterial tests is microdilution, since this method allows obtaining MIC chased M. recutita flowers against P. aeruginosa, S. aureus, E. coli and S.
and minimum bactericidal concentration (MBC) values. This technique enterica subsp. enterica serovar Typhimurium. Their tests were per-
was used together with the antiadherence assay to observe if the M. formed through two techniques, the broth dilution, where the MIC was
recutita hydroethanolic extract had this property in human colon car- obtained, and diffusion in agar. The results of this study showed that
cinoma cells affected by Campylobacter jejuni (Bensch et al., 2011). The the ethanolic extract has antibacterial activity against P. aeruginosa in
results evidenced small degree of antiadhesive activity which was both techniques, presenting a MIC value of 1 g/mL and an inhibition
considered non-significant, since its IC50 was higher than 35 mg/mL. halo of 10 mm greater than the positive control (disk containing alcohol
Alternatively, when the M. recutita hydroethanolic extract was tested at 70%). The MIC value obtained is considered high, which could justify
against two strains of bacteria causing gastrointestinal diseases, Heli- the inhibition of bacterial growth only in the crude extract. As for the
cobacter pylori and C. jejuni, the extract presented a very satisfactory cyclohexane extract, P. aeruginosa showed resistance in both techni-
result against C. jejuni, showing 100% inhibition at 20 mg/mL (Cwikla ques. Neither extracts showed significant activity against any other
et al., 2010). In another work, the in-vitro antimicrobial action of the bacteria evaluated. In another study, a 50% hydroalcoholic extract of
essential oil of M. recutita together with other plant species against M. recutita extracts was fractionated by overpressured-layer chromato-
microorganisms obtained from patients diagnosed with external otitis graphy (OPLC) to evaluate the antibacterial activity against Bacilus
were evaluated (Nogueira et al., 2008). The isolated bacteria were from subtilis and Pseudomonas syringae pv. maculicola by means of the in vitro
12 strains of Pseudomonas aeruginosa and 8 strains of Staphylococcus direct bioautography methodology (Moricz et al., 2012). Both flowers
aureus. The inhibition halo (mm) of this essential oil showed no in- and leaves inhibited the growth of P. syringae, and some of the eleven
hibitory effect against P. aeruginosa strains (0 mm), although at the fractions tested presented antibacterial activity. The extracts were
concentration of 4% of this oil, it was possible to inhibit the growth of tested against the following bacteria: B. subtilis, S. aureus, methicillin-
three S. aureus strains (halo of 10 mm). In this study, the positive resistant S. aureus (MRSA), Staphylococcus epidermidis, P. syringae pv.
control was that of the microorganism in the culture medium in the maculicola, Xanthomonas campestris pv. vesicatoria, E. coli, and Aliivibrio
absence of antimicrobials, and no antibiotic was used as reference. In fischeri (Jesionek et al., 2015). The extracts showed antibacterial ac-
spite of, the results of this study showed that the essential oil from M. tivity against S. aureus and S. epidermidis strains, both with inhibition
recutita presented notable antimicrobial effects on some germs that zones of 7 mm, a weak activity against MRSA (6 mm), while the activity
cause external otitis (Nogueira et al., 2008). against E. coli was not analyzed. The values of the gentamicin control
Munir et al. (2014), using the cavity diffusion methodology, used were 7 mm and 6 mm for S. aureus and S. epidermidis, respectively, and
the ethanolic and methanolic extracts from roots of M. recutita against vancomycin showed no activity against the aforementioned bacteria.
S. aureus, E. coli and Salmonella typhi. Both the ethanolic and methanolic Also, through direct bioautography and thin layer chromatography

83
M. Sharifi-Rad et al. Microbiological Research 215 (2018) 76–88

plate visualization, in vitro evaluation, isolation and separation of the replace synthetic compounds and guarantee food safety and quality. In
bioactive components of the M. recutita dye were carried out. The this framework, the addition of different natural extracts (from plants,
presence of two active components, apigenin and α-linolenic acid, was spices and fruits) as preservatives is a strategy already developed in
confirmed by LC/MS (Jesionek et al., 2015), which may be responsible bakery, meat and dairy products (Burt, 2004; Reddy et al., 2005;
for the antibacterial activity (Jung et al., 2015; Akilandeswari and Rasooli, 2007; Shah et al., 2014). However, applications that involve
Ruckmani, 2016). These are some examples of how the use of different chamomile are still scarce.
parts of plant, different solvents and different extraction techniques In fact, while many studies reported its antioxidant and anti-
affect chemical composition of extracts and therefore their antibacterial microbial activity in in vitro systems, as previously discussed, only few
activity. researches focused on the validation of this potential in food matrices.
In addition to terpenoids, flavonoids or coumarins, other acid This is a critical aspect, since literature reported that essential oils can
compounds have bee also suggested to play a role in the antibacterial interact with food constituents (fat, starch, protein), thus significantly
effect. I this sense, it is well established that endodontic instrumenta- reducing their bioactivity (Hyldgaard et al., 2012). Therefore, the ex-
tion causes a smear covering the surfaces of the root canal, which can trapolation of results from in vitro tests to real systems is often difficult
be colonized by bacteria such as Enterococcus faecalis. Interestingly, a M. and data obtained in vitro need to be validated in foods, since lower
recutita hydroalcoholic extract was used together with tooth roots ex- activity is likely. Applications available in the current literature involve
tracted from patients. In addition to chamomile, a sodium hypochlorite dairy products such as cottage cheese (Caleja et al., 2016) and bakery
solution (2.5%) was used, which had already been disinfected, since it products, i.e., biscuits (Caleja et al., 2017). Regarding dairy, the first
is used as an irrigant for this treatment and the solution of MTAD study (Caleja et al., 2015) investigated the addition of chamomile ex-
(composed by a mixture of tetracycline isomer, an acid and a de- tracts obtained by decoction on physic-chemical parameters and nu-
tergent). The extract was more effective in the disinfection process than tritional composition of cottage cheese, as well as its shelf-life, respect
the commonly used sodium hypochlorite solution. In the discussion, to a control cheese without any additive. The results showed that M.
this cleaning function is assigned to various acids present in the plant, recutita extracts did not significantly modify nutritional and fatty acid
for example, capric acid and caprylic acid (Venkataram et al., 2013). In profiles but improved antioxidant potential (lower lipid peroxidation,
another work, Lins et al. (2013) evaluated the effect of mouthwashes higher free radical scavenging activity) and prolonged shelf-life, since
based on the chamomile flower hydroalcoholic extract. All mouthwa- only in control samples degradation after 14 days of storage was evi-
shes, chamomile and chlorhexidine as control, significantly reduced dent. This bioactivity is due to the release during decoction of phenolic
bacterial plaque, and chamomile was the one that had the greatest compounds, which can exert antioxidant and antimicrobial activities. In
plaque reduction, but not significantly different compared to control. a following study, the same authors (Caleja et al., 2016) used chamo-
When linking ethnobiological reports with research on the eluci- mile extracts, microencapsulated in alginate before incorporation into
dation of antibacterial biological activity of the genus, only the po- cottage cheese, in order to prevent phenolic compound degradation and
tential of M. recutita has been evaluated. None of the latter studies therefore extend their bioactivity over storage. Samples with free ex-
evaluated the aqueous extract, which is the main form of use by the tracts were also prepared and results demonstrated that “functionalized
population. However, other types of extracts and essential oils have cheeses” had higher antioxidant activity but similar color parameters
demonstrated antibacterial activity, indicating that the plant has active and nutritional and fatty acid profiles. Moreover, the microencapsula-
chemical constituents capable of interfering with bacterial growth and tion was able to prolong antioxidant activity, since microencapsulated
scientifically justifying the folk use of this species. Anyway, some stu- extracts showed higher antioxidant activity after 7 days of storage. This
dies are contradictory and, probably, it is due to the different compo- technique could be a strategy to preserve natural extracts potential
sition of the essential oils and extracts studied. More studies about the during long storage of food products, reducing also the organoleptic
synergy of the plant extracts components on their antibacterial activity impact of these substances.
are needed besides evaluate if it is a better economic option the ex- As far as bakery products, to our knowledge the only application
traction of the components of the plant or their organic synthesis. The reported up to now is the addition of chamomile extracts (obtained by
promising results of Matriarca genus as antimicrobial offer prospects for decoction) as antioxidant agents in wheat biscuits (Caleja et al., 2017),
further research, as the evaluation of the biological potential of the in comparison with synthetic compounds and control biscuits (without
major components and the elucidation of their molecules, may, in the antioxidant addition). Samples were analyzed during 60 days storage to
future, contribute to the discovery of effective antibacterial components monitor nutritional profile, sugars, fatty acids and antioxidant activity.
derived from plants for the treatment of bacterial diseases or techno- The results showed that the incorporation of natural or synthetic ad-
logical applications as food preservative. ditives did not significantly modify color or nutritional profile of bis-
cuits, if compared to control samples. Interestingly, the natural and
6. Essential oil obtained from genus Matricaria plants as a food synthetic additives gave similar antioxidant activity; therefore, these
preservative natural extracts seem to be a good replacer for foods without synthetic
additives that could fulfill the increasing request of consumers for
Throughout the history, chamomile, and particularly M. recutita, has healthy and “natural” products.
been one of the most used and popular medicinal plants due to the Another application of this plant as food preservative could be its
richness in active compounds. Its inflorescences contain over 120 incorporation in antimicrobial active packaging. In a study performed
constituents that can exert several functional activity such as anti- by Aliheidari et al. (2013), M. recutita essential oil was added at 1% (v/
oxidant (Hernández-Ceruelos et al., 2010) and antimicrobial (Silva v) in a casein-based film to increase its barrier properties (higher
et al., 2012) properties. Among them, the antibacterial activity of this thickness and lower water vapour permeability, because of its lipidic
genus has been well studied, either in the search for new compounds nature) and antimicrobial activity. The film obtained showed an in-
capable of decreasing the bacterial resistance that is rapidly and con- hibitory effect against L. monocytogenes, S. aureus, and E. coli in vitro
tinuously growing, or to reduce the contamination caused by bacteria in (evaluated by disk-diffusion method), and this antibacterial activity
food, dental appliances, as noted above, and others. was attributed to the essential oil components, such as α-bisabolol.
Therefore, extracts derived from M. recutita can be used in food Using again the same methodology, the antibacterial activity of the
products for two main properties: antioxidant and antimicrobial activ- essential oil obtained from M. recutita flowers and its main compound
ities. Nowadays, the increasing demand of consumers for “natural” trans-β-farnesene were tested to evaluate their use in food instead of
foods, due to a higher sensitivity to nutritional and ethical aspects, has chemical additives (Soković et al., 2010). In addition to the afore-
enhanced the need of industry to look for natural substances able to mentioned bacteria, the essential oil presented lower antibacterial

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M. Sharifi-Rad et al. Microbiological Research 215 (2018) 76–88

activity against B. subtilis, Enterobacter cloacae, Micrococcus flavus, Pro- purposes and food applications. These studies should be addressed at
teus mirabilis, P. aeruginosa, Salmonella enteritidis, S. epidermidis, and S. the same time than the scientific demonstration of its bioactivity in a
typhimurium, in comparison with other studied plants and the control clinical context or in the food matrix.
(the antibiotic streptomycin). As for P. mirabilis and P. aeruginosa, the Nevertheless, M. recutita seems to have promising potential in food
oil had no effect. In this same study, the microdilution test was per- applications: essential oils or aqueous extracts may be incorporated in
formed to obtain the MIC values (7–10 μg/mL) and MBC (8–15 μg/mL) foods to increase oxidation stability and shelf-life and as antimicrobial
of the essential oil, requiring higher levels than those of streptomycin active packaging with improved barrier properties, shelf-life and safety.
(1–2 μg/mL) (Soković et al., 2010). This opens interesting scenarios for Therefore, as commented above the chemical composition of M. recutita
the application of this essential oil in food packaging to prolong shelf- essential oils or extracts when using in food should be evaluated, as well
life and increase safety. However, a similar research focused on the as the organoleptic properties that these constituents may confer. In this
addition of different essential oils to sodium alginate/glycerol films regard, microencapsulation could be used as a strategy to control the
evidenced that chamomile blue was the only essential oil ineffective release of bioactive compounds during long storage of food products
against E. coli and Candida albicans, independently of the concentration and reduce the organoleptic impact of these substances. Moreover, M.
used (Liakos et al., 2014). This can be due to the variability of essential recutita extracts and essential oils have demonstrated antibacterial ac-
oil compositions, which is known to be one of the main limitations for tivity, with interest in oral health. Anyway, some studies are contra-
their use in food industry (Hyldgaard et al., 2012). dictory and they should be reinforced together with a compositional
The use of essential oils in food is common due to the interest in evaluation to understand these differences.
obtaining a specific taste. Several reports suggest that the use of es-
sential oils as antimicrobial agents may improve food safety and is well Disclosure of interest
documented in model food systems or in real food (Friedman et al.,
2002; Soković et al., 2010). Also, the majority of the essential oil are The authors declare that they have no conflicts of interest con-
classified as Generally Recognized As Safe (GRAS), including M. cha- cerning this article.
momilla (Food and Drug Administration, 2017). Although their use in
foods may be limited due to flavor considerations because effective Acknowledgements
antimicrobial doses may exceed organoleptically acceptable levels.
Therefore, there is an increasing demand for accurate knowledge of the We are grateful to anonymous Reviewers for providing constructive
MIC values of essential oils to enable a balance between the anti- criticism on the manuscript. A. Sureda was supported by Instituto de
microbial efficacy in the food matrix and sensory acceptability (Soković Salud Carlos III (CIBEROBN CB12/03/30038).
et al., 2010).
Even if food applications are still scarce, M. recutita seems to have References
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